Basal temporal sulcal morphology in healthy controls and

Basal temporal sulcal morphology in
healthy controls and patients with
temporal lobe epilepsy
H. Kim, MSc
N. Bernasconi, MD,
PhD
B. Bernhardt, MSc
O. Colliot, PhD
A. Bernasconi, MD
Address correspondence and
reprint requests to Dr. Andrea
Bernasconi, Montreal
Neurological Institute, 3801
University Street, Montreal,
Quebec, Canada H3A 2B4
[email protected]
ABSTRACT
Background: We previously demonstrated that shape variants of the hippocampal formation are
more prevalent in patients with temporal lobe epilepsy (TLE) than in healthy individuals.
Objective: To categorize sulcal patterns of the basal temporal lobe in TLE compared to healthy
controls.
Methods: We studied 51 healthy controls and 69 patients with TLE (37 left, 32 right TLE). Brain
sulci were identified and labeled automatically on MRI using an algorithm based on a congregation
of neural networks that allows mapping three-dimensional sulcal models on the cortical surface.
We used four sulcal patterns classes to categorize the sulcal arrangement in the inferior surface
of the temporal lobe in each subject: Type 1, i.e., single-branch, unbroken collateral sulcus (CS)
connected with the rhinal sulcus (RS) anteriorly; Type 2, i.e., CS connected with the occipitotemporal sulcus (OTS), but separated from the RS; Type 3, i.e., CS separated from the OTS and RS,
which are connected; and Type 4, i.e., CS, OTS and RS separated.
Results: In healthy controls, Type 1 and Type 2 were the patterns seen most frequently. Overall,
82% (42/51) of subjects had the same sulcal pattern in both temporal lobes. Inter-rater reliability
for 35 randomly selected subjects indicated excellent agreement (Cohen’s Kappa: 0.84). Compared to controls, we found an increased frequency of Type 1 CS in patients with TLE, both in the
left (77% vs 47%, p ⫽ 0.004) and the right hemispheres (72% vs 41%, p ⫽ 0.002). On the other
hand, we found a decreased frequency of Type 2 CS in patients with TLE, both in the left (4% vs
31%, p ⫽ 0.00002) and the right hemisphere (4% vs 35%, p ⬍ 0.00001).
Conclusions: A single-branch, unbroken collateral sulcus is the predominant sulcal pattern found
in temporal lobe epilepsy. This “simplified” arrangement may be an indicator of neurodevelopmental deviance associated with this condition. Neurology® 2008;70:2159–2165
GLOSSARY
CS ⫽ collateral sulcus; OTS ⫽ occipitotemporal sulcus; RS ⫽ rhinal sulcus; TLE ⫽ temporal lobe epilepsy.
Temporal lobe epilepsy (TLE) is the most common medically intractable partial epilepsy
in adults. Although hippocampal atrophy on MRI is a hallmark of the disorder in the
majority of cases, several studies have confirmed that pathology in TLE extends to extrahippocampal mesial limbic structures such as the entorhinal cortex.1-4
The vast majority of MRI studies in TLE have been focused on assessing changes in
gray and white matter volumes. Other aspects of cortical morphology such as sulcal
shape, positioning, and patterning may give additional insights on structural brain
changes associated with TLE. There is growing evidence that developmental hippocampal abnormalities increase susceptibility to seizures and neuronal loss, and may facilitate
subsequent hippocampal sclerosis in patients with TLE.5 We previously demonstrated
that shape and positioning variants of the hippocampal formation are more prevalent in
patients with epilepsy than in healthy individuals, and are found in a similar proportion
From the Department of Neurology (H.K., N.B., B.B., A.B.), McGill University, Montreal Neurological Institute, Quebec, Canada; and
Cognitive Neuroscience and Brain Imaging Laboratory (O.C.), CNRS, Hôpital de la Salpêtrière, Paris, France.
Funded by a grant from the Canadian Institutes of Health Research (CIHR-MOP 57840). B.B is supported by the German National Merit
Foundation, Bonn, Germany.
Disclosure: The authors report no disclosures.
Copyright © 2008 by AAN Enterprises, Inc.
2159
in those with malformations of cortical development and TLE.6 In addition, atypical
morphologies of the collateral sulcus (CS)
have been described in relation to anomalous hippocampal shape and positioning.6,7
Morphologic MRI studies of sulcal
patterns using cortical surface rendering
techniques have provided evidence for
neurodevelopmental deviance in several
neurologic disorders, including schizophrenia 8 and Williams syndrome. 9 In
TLE, one previous study 10 categorized
the CS into three types according to its
relationship to the rhinal sulcus. In that
2D MRI study, which did not include
healthy control subjects, no predominant
sulcal pattern was found.
Although MRI offers an opportunity to
complement labor-intensive postmortem
studies of cortical anatomy, the complexity
of the brain’s convolution makes the visual
identification of sulcal-gyral abnormalities
difficult on orthogonal planes obtained in
conventional MRI. To bypass this disadvantage, precise and robust computerbased sulcal identification techniques have
been developed to allow sulcal pattern
analysis and automatic labeling on the
brain surface.11
In the present study, we sought to investigate the morphologic sulcal patterns of the
medio-basal temporal lobe on MRI using an
automated sulcal extraction method. We
chose to study the collateral sulcus and the
occipito-temporal sulci, which are the major
landmarks separating the lateral and mesial
temporal lobe. The collateral sulcus borders
the entorhinal and perirhinal cortices,12
which have a strong functional connection
with the hippocampus13 and are involved in
the epileptogenic network in TLE.
METHODS Subjects. We randomly selected 69 patients
with unilateral medically intractable TLE (33 men; mean age
⫽ 32 ⫾ 9 years, range ⫽ 16 – 49) and no mass lesion (obvious
malformations of cortical development, tumor, or vascular
malformations) on MRI from our database. The control
group consisted of 51 healthy subjects (25 men; mean age ⫽
32 ⫾ 11 years, range ⫽ 20 –56). Demographic and clinical
data were obtained through interviews and hospital chart
reviews. The Ethics Committee of the Montreal Neurological Institute and Hospital approved the study and written
informed consent was obtained from all participants.
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Neurology 70
May 27, 2008 (Part 2 of 2)
TLE diagnosis and lateralization of the seizure focus
were determined by comprehensive evaluation, including detailed seizure history and semiology, neurologic examination, video-EEG telemetry, and neuropsychological
evaluation in all patients. Based on these criteria, patients
were divided into those with a left-sided (LTLE, n ⫽ 37) or a
right-sided (RTLE, n ⫽ 32) seizure focus.
Forty-four patients were operated (44/69 ⫽ 64%). The
mean postsurgical follow-up was 3.4 years (range: 1 to 6
years). Twenty-five patients underwent a selective amygdalo-hippocampectomy: 20 had an outcome of Engel class
I,14 4 had a class II, and 1 a class III outcome. Qualitative
pathologic examination of the resected tissue revealed hippocampal sclerosis in 19 patients and specimens were not
sufficient for review in the other six. Nineteen patients had
an amygdalo-hippocampectomy with temporal cortical resection: 13 became seizure free (Engel class I), 1 had class II,
and 5 class III outcome. Qualitative histopathology showed
hippocampal sclerosis in 12 patients, which was associated
with neocortical dyslamination and columnar disorganization in 2, and gray matter gliosis in 2 others. Gliosis of the
cortical gray matter was seen in 2 patients and heterotopic
neurons in the temporal lobe white matter in another. Due to
subpial aspiration, specimens were unsuitable for histopathology in 4 patients.
MRI acquisition and image preprocessing. In all subjects, images were acquired on a 1.5 T Gyroscan (Philips
Medical System, Eindhoven, Netherlands) using a threedimensional T1-fast field echo sequence (repetition time ⫽
18, echo time ⫽ 10, 1 acquisition average pulse sequence, flip
angle ⫽ 30º, matrix size ⫽ 256 ⫻ 256, field of view ⫽ 256,
slice thickness ⫽ 1 mm). This high-resolution T1-weighted
three-dimensional gradient-echo sequence provides exquisite
anatomic details with an isotropic voxel size of 1 ⫻ 1 ⫻ 1 mm
and features high signal-to-noise and contrast-to-noise.15
Each image underwent automated correction for intensity non-uniformity and intensity standardization. Images
were then registered into a standardized stereotaxic coordinate space based on the Talairach atlas16 to adjust for differences in total brain volume and brain orientation and to
facilitate the identification of boundaries by minimizing
variability in slice orientation.17 This procedure uses an automatic, multiscale feature-matching algorithm17 that performs a 9-parameter linear transformation to match each
brain to a template brain.
Automatic sulcal extraction and labeling. Generation of brain surfaces and sulcal models. For sulcal extraction, images were processed using BrainVISA, a brain image
analysis software that allows the user to reconstruct the surfaces corresponding to GM-WM and GM-CSF interfaces
and to extract the brain sulci.11 To compute accurate cortical
surfaces and brain sulcal folds, image processing includes the
following steps: 1) brain segmentation; 2) classification of
WM, GM, and CSF generating separate maps in each hemisphere; 3) reconstruction of the surfaces corresponding to
the GM-WM and GM-CSF interface using the above classification maps; 4) extraction of the sulcal folds by segmenting
the skeletonized GM/CSF interface into simple surfaces.
Sulcal labeling. After extraction, sulci are automatically
labeled using a congregation of neural networks trained on a
manually identified database of sulci.11 Recognition of structures is achieved by maximizing similarity of sulci features
and sulci relations.
Figure 1
Three-dimensional surface rendering (A) and coronal MRI slices of the basal temporal lobe (B) showing
the collateral sulcus (CS, red), rhinal sulcus (RS, blue), and occipitotemporal sulcus (OTS, green)
AM ⫽ amygdala; HH ⫽ hippocampal head; HB ⫽ hippocampal body; HT ⫽ hippocampal tail.
Categorization of sulcal patterns of the basal temporal lobe. The ventral and medial surfaces of the temporal lobe are organized into strips by two prominent
rostrocaudally oriented sulci. The more lateral of the two is
the occipitotemporal sulcus (OTS), which is often broken
forming small, transverse gyri. The more medial is the collateral sulcus (CS) and marks the border between the parahippocampal gyrus and the occipitotemporal (i.e., fusiform)
gyrus. The CS may be continuous rostrally with the rhinal
sulcus (RS).18 Figure 1shows the various sulci on orthogonal
MRI slices and a three-dimensional MRI surface rendering.
The normal sulcal anatomy of the inferior surface of the
temporal lobe includes four main patterns based on the relationship between the CS and neighboring sulci, i.e., the RS
and OTS.19 We used these four pattern classes to describe the
sulcal arrangement in each subject as shown in figure 2:
Table
Frequencies of sulcal pattern types in the basal temporal lobe in healthy
controls and patients with temporal lobe epilepsy (TLE)
Sulcal pattern
Healthy controls (n ⫽ 51)
Patients with TLE (n ⫽ 69)
Left
Left
Right
Right
Type 1: CS connected with the RS 47% (24/51) 41% (21/51) 77%* (53/69) 72%* (50/69)
Type 2: CS connected with the
OTS, but separated from the RS
Type 3: CS separated from the
OTS and RS, which are connected
Type 4: CS, OTS, and RS
separated
31% (16/51) 35% (18/51)
6% (3/51)
16% (8/51)
4%† (3/69)
4%† (3/69)
9% (6/69)
12% (8/69)
20% (10/51) 10% (7/69)
12% (8/69)
4% (2/51)
*p ⬍ 0.005; †p ⬍ 0.00005.
CS ⫽ collateral sulcus; OTS ⫽ occipitotemporal sulcus; RS ⫽ rhinal sulcus.
• Type 1: single-branch, unbroken CS connected with
the RS anteriorly
• Type 2: CS connected with the OTS, but separated
from the RS
• Type 3: CS separated from the OTS and RS, which are
connected
• Type 4: CS, OTS, and RS separated
MR images were numerically coded and presented in
random order on a console independently to the observers
unaware of the clinical information. The left and right hemispheres were analyzed separately.
MRI volumetry. Volumetric analysis of the hippocampus
was performed manually according to our previously published protocol.1 Based on a 2 SD cutoff from the mean of
healthy controls, 36/69 (52%) patients with TLE had hippocampal atrophy and 33/69 (48%) normal hippocampal
volumes.
Statistical analysis. We evaluated associations between
CS branch types in each hemispheres and groups (healthy
controls and patients with TLE), gender, side of seizure focus, and history of febrile seizures using ␹2 test for categorical data analysis. Associations between CS branching types
and hippocampal volume were also analyzed in the same
way.
Two raters (H.K. and B.B.) analyzed 35 randomly selected subjects (i.e., 70 hemispheres), including patients of all
categories and healthy controls. We assessed the chancecorrected inter-rater agreement between the two observers
by computing Cohen’s Kappa.
RESULTS The two raters differed only in 3 of the
70 possible ratings. We obtained a chanceNeurology 70
May 27, 2008 (Part 2 of 2)
2161
Figure 2
more frequently associated with men than women
(58/66 ⫽ 88% vs 45/72 ⫽ 63%, p ⫽ 0.001) and
Type 4 with women than men (14/72 ⫽ 19% vs
4/66 ⫽ 6%, p ⫽ 0.03). There was no relationship
between sulcal patterns and seizure focus lateralization, or any associations between CS sulcal
patterns and hippocampal volume. Likewise, we
found no association between sulcal patterns and
history of febrile seizures.
Sulcal pattern classes
Upper panels: basal view of the three-dimensional MRI rendering with sulci mapped on the
cortical surface. Middle panels: extracted sulci, i.e., collateral sulcus (CS, red), rhinal sulcus
(RS, blue), and occipitotemporal sulcus (OTS, green). Lower panels: three coronal MRI slices
with sulci marked at the level of hippocampal head, body, and tail at the level indicated by the
Talairach coordinates in coronal plane (y) on the middle panels (dashed line). Sulcal pattern
classes: (A) Type 1: one-branch CS connected with RS; (B) Type 2: two-branch CS connected
with OTS in its posterior portion; (C) Type 3: two-branch CS having connection between RS
and OTS in its anterior portion; (D) Type 4: three-branch CS with no connection between the
sulci.
corrected Cohen’s ␬ ⫽ 0.84, which represents excellent agreement.
Frequencies of the various sulcal pattern types
in controls and patients with TLE are presented in
the table. In healthy controls, Type 1 and Type 2
were the patterns seen most frequently. Overall,
82% (42/51) of subjects had the same sulcal pattern in both temporal lobes. There was no association between any sulcal pattern type and gender.
Compared to controls, in patients with TLE
we found the following: 1) an increased frequency
in pattern Type 1 (single-branch, unbroken CS
connected with the RS) in the left (77% vs 47%;
␹2 ⫽ 8.2, df ⫽ 1, p ⫽ 0.004) and right hemisphere
(72% vs 41%; ␹2 ⫽ 9.2, df ⫽ 1, p ⫽ 0.002); 2) a
decreased frequency of sulcal pattern Type 2 (CS
connected with the OTS, but separated from the
RS) in the left (4% vs 31%; ␹2 ⫽ 17.0, df ⫽ 1, p ⫽
0.00002) and the right hemisphere (4% vs 35%; ␹2
⫽ 19.1, df ⫽ 1, p ⬍ 0.00001). There was no group
difference in the frequency of Type 3 and 4 sulcal
patterns. A total of 77% (53/69) of patients had
the same sulcal pattern in both temporal lobes. In
relation to gender, sulcal pattern Type 1 was
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Neurology 70
May 27, 2008 (Part 2 of 2)
DISCUSSION Studying the morphologic patterns
of the inferior surface of the temporal lobe in
healthy controls and patients with TLE, we found
that more than 70% of patients with TLE exhibit
a single-branch, unbroken CS connected with the
RS. On the other hand, more than half of the controls presented with patterns displaying a lack of
continuity between these two sulci. In particular,
a Type 2 CS connected with the OTS, but separated from the RS, was more common in healthy
controls than in patients. Cortical complexity can
be described by the spatial frequency of fissuration.20 When this criterion is applied to compare
sulcal patterns among our subjects, Type 1 CS appears as “simplified,” since its relationship with
the surrounding sulci produces a low degree of
complex arrangement (figure 1).
During the initial phase of brain development,
the surface of the hemispheres is smooth. Most
sulci and gyri develop during the third trimester,
and the primary and secondary fissures are visible
at birth.19,21 Typically, the major sulci continue to
develop after birth22 and during early childhood
the degree of gyrification stabilizes.23 Sulcal patterns are an effect of the expansion of cortical
gray matter and the development of interconnecting circuits. Mechanisms leading to cortical folding involve mechanical forces resulting from
different tension of growth between early cortical
strata,24 tension along axons between interactive
cortical areas,25 and changes in subcortical connectivity patterns.26 A variety of non-genetic factors, including intrauterine environment,27,28
modulate hemispheric sulcal morphology, while
data from morphologic analysis of individual
sulci suggest genetic encoding.29 The CS is among
the deep sulci that appear early during human
gestation, around the 23rd week of gestation.21
In non-diseased brains, postmortem studies
have reported variable folding patterns in the inferior surface of the temporal lobe. A study of 25
brains19 described CS categories based on its connection patterns to the neighboring sulci and
found that the CS was connected with the RS in
26% of the specimens. In another observation,30
only one out of the five brains examined presented with an unbroken long collateral sulcus
extending into the uncal region. The limited number of brain specimens included in these studies
could explain the relatively low percentages compared to our results. To our knowledge, CS has
been previously studied in healthy subjects only
once using in vivo high-resolution MRI.31 Our
findings are in agreement with this study that
used a similar number of subjects and showed an
unbroken single-branch CS connected with the
RS in about 45% of individuals. This study also
reported comparable proportions of Type 2 and
Type 3 CS in about 35%, and Type 4 in 20% of
subjects.
Type 1 single-branch, unbroken long CS connected with the RS was present in more than 70%
of our patients with TLE, while Type 2 (i.e., CS
connected with the OTS, but separated from the
RS) was found in only 4% of them. Sulcal anatomy of the basal temporal lobe in TLE has been
assessed only in one previous study10 in which a
CS Type 1 was seen in 33% of the patients. This
low incidence is most likely explained by the use
of coronal, low-resolution MRI, potentially leading to incorrect determination of sulcal depth,
connective patterns, and interruptions. Our highresolution MRI protocol with 1 mm isotropic
voxels and no interslice gap allowed for an improved in vivo identification of sulcal patterns.
Furthermore, the combination with advanced image processing enabled us not only to inspect
brain surfaces in a similar way as in postmortem
studies, but also to evaluate the morphology by
means of three-dimensional sulcal models. Importantly, the comparison with healthy controls
allowed us to establish that Type 1 CS is the predominant sulcal pattern in TLE. In our patients,
we did not find any association with sulcal patterns and the side of the seizure focus, indicating
that the location of the epileptogenic focus and
morphologic changes may not necessarily overlap.
Other brain pathologies unrelated to epilepsy
have been associated with particular constellations of sulcal morphology. Atypical configurations of the diagonal sulcus, a secondary sulcus
bifurcating the pars opercularis of Broca area in
two segments, have been seen more often in
adults with persistent developmental stuttering
than in healthy controls, suggesting that this sulcal morphology may be adequate to support the
development of language, but may put individuals at risk for developmental stuttering.32 Sylvian
fissure variants have been found more frequently
in the right hemisphere of patients with Williams
syndrome than in controls.33 Reduced frequency
of the paracingulate sulcus has been reported in
schizophrenia.34 Generally, sulcal variants in
these conditions have been considered to be indicators of neurodevelopmental deviance.
Perturbation in connections may alter the mechanical tension that has been hypothesized as required for normal development of cortical
folding.25 Experimental data indicate that early
disruption in connectivity can lead to the emergence of anomalous sulcal patterns.26 Altered sulcal patterns in epilepsy are usually found in
patients with malformations of cortical development. In the absence of an obvious malformation,
unusual sulcal patterns are thought to be a
marker of subtle cortical dysgenesis.35 Some patients with refractory TLE and hippocampal sclerosis also have radiologically detected dysplastic
abnormalities36 and are regarded as examples of
dual pathology. However, even when MRI reveals no evidence of an evident malformation,
histopathology may show microscopic dysplasia
in the neocortical tissue of about 40% of patients
with TLE with hippocampal sclerosis.37 These
mild structural abnormalities reflect a spectrum
of developmental changes, typically involving the
architectonic cortical organization, such as laminar disarray, abnormal neuronal aggregates, dysmorphic neurons, and neuronal glial clustering,
and are not related to febrile seizures.38 Therefore, our findings give rise to the question as to
whether in TLE the “simplified” Type 1 CS may
be the marker of a subtle developmental structural abnormality of the temporal lobe.5,7
Although a given sulco-gyral pattern may be
more prevalent in patients than in healthy individuals, its impact in epilepsy is not yet determined. In TLE, several authors have suggested
that a pre-existing abnormality constitutes a susceptibility factor predisposing the temporal lobe
to insults, thereby triggering the epileptogenic
process. Developmental dysplastic lesions have
been proposed as candidates, because these malformations are clearly present before the onset of
epilepsy.39 We previously demonstrated that
shape variants of the hippocampal formation are
found more frequently in patients with obvious
cortical malformations and in TLE with hippocampal sclerosis than in healthy controls. We
postulated that in TLE these changes may be indicators of a disorder of brain development and
may promote epileptogenesis. Similarly, a singlebranch, unbroken CS may leave the temporal lobe
of some patients with TLE more vulnerable to
Neurology 70
May 27, 2008 (Part 2 of 2)
2163
precipitating injuries occurring as early as the
third trimester of gestation. An early nature of
these events in our patients is supported by our
results showing the lack of relationship between
sulcal morphology and history of febrile seizures.
The predominant “simplified” Type 1 CS
found in TLE may be the result of various overlapping mechanisms including incomplete maturation and variations in the underlying, possibly
disturbed neuronal connectivity in areas adjacent
to the CS known to be involved in the epileptogenic network in TLE, namely the entorhinal and
perirhinal cortices.1,40 Future studies are needed to
determine the relationship between MRI and histologic findings in order to clarify the spectrum of
developmental abnormalities and their significance in the genesis of seizures in TLE.
10.
11.
12.
13.
14.
ACKNOWLEDGMENT
The authors thank Prof. Gary Van Hoesen for comments on the
manuscript.
Received May 29, 2007. Accepted in final form November
21, 2007.
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